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Conserved white rot enzymatic mechanism for wood decay in the Basidiomycota genus Pycnoporus

Shingo Miyauchi 1, 2 Hayat Hage 1 Elodie Drula 1 Laurence Lesage-Meessen 3, 1 Jean-Guy Berrin 1 David Navarro 3, 1 Anne Favel 1 Delphine Chaduli 3, 1 Sacha Grisel 1 Mireille Haon 1 François Piumi 1 Anthony Levasseur 4, 5 Anne Lomascolo 1 Steven Ahrendt 6 Kerrie Barry 6 Kurt Labutti 6 Didier Chevret 7 Chris Daum 6 Jérôme Mariette 8 Christophe Klopp 8 Daniel Cullen 9 Ronald de Vries 10, 11 Allen Gathman 12 Matthieu Hainaut 13 Bernard Henrissat 13 Kristiina Hildén 11 Ursula Kues 14 Walt Lilly 12 Anna Lipzen 15 Miia Mäkelä 11 Angel Martinez 16 Melanie Morel-Rouhier 2 Emmanuelle Morin 2 Jasmyn Pangilinan 17 Arthur Ram 18 Han Wösten 19 Francisco Ruiz-Dueñas 16 Robert Riley 15 Eric Record 1 Igor Grigoriev 20 Marie-Noelle Rosso 1
Abstract : White-rot (WR) fungi are pivotal decomposers of dead organic matter in forest ecosystems and typically use a large array of hydrolytic and oxidative enzymes to deconstruct lignocellulose. However, the extent of lignin and cellulose degradation may vary between species and wood type. Here we combined comparative genomics, transcriptomics and secretome proteomics to identify conserved enzymatic signatures at the onset of wood decaying activity within the Basidiomycota genus Pycnoporus. We observed strong conservation in the genome structures and the repertoires of protein coding genes across the four Pycnoporus species described to date, despite the species having distinct geographic distributions. We further analyzed the early response of P. cinnabarinus, P. coccineus and P. sanguineus to diverse (ligno)-cellulosic substrates. We identified a conserved set of enzymes mobilized by the three species for breaking down cellulose, hemicellulose and pectin. The co-occurrence in the exo-proteomes of H2O2 producing enzymes with H2O2 consuming enzymes was a common feature of the three species, although each enzymatic partner displayed independent transcriptional regulation. Finally, cellobiose dehydrogenase-coding genes were systematically co-regulated with at least one AA9 LPMO gene, indicative of enzymatic synergy in vivo. This study highlights a conserved core white-rot fungal enzymatic mechanism behind the wood decaying process.
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Submitted on : Monday, June 15, 2020 - 2:07:10 PM
Last modification on : Wednesday, May 12, 2021 - 8:13:43 AM

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Shingo Miyauchi, Hayat Hage, Elodie Drula, Laurence Lesage-Meessen, Jean-Guy Berrin, et al.. Conserved white rot enzymatic mechanism for wood decay in the Basidiomycota genus Pycnoporus. DNA Research, Oxford University Press (OUP), 2020, ⟨10.1093/dnares/dsaa011⟩. ⟨hal-02868456⟩

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